Advertisement

Ecotoxicology

, Volume 7, Issue 5, pp 259–278 | Cite as

A Population Genetic Analysis of the Potential for a Crude Oil Spill to Induce Heritable Mutations and Impact Natural Populations

  • Matthew A. Cronin
  • John W. Bickham
Article

Abstract

The primary environmental impact following an oil spill typically is acute toxicity to fish and wildlife. However, multigenerational effects through toxicant-induced heritable mutations might also occur. Some polycyclic aromatic hydrocarbon (PAH) components of crude oil are potentially mutagenic, although specific components and doses that induce mutations are poorly known. We applied population genetics concepts to assess the extent of mortality and the persistence of deleterious heritable mutations resulting from exposure to potential mutagens, such as crude oil. If lethal mutations are induced, the population will experience some mortality, but the mutations are quickly removed or reduced to low frequency by natural selection. This occurs within one or a few generations when mutations are dominant or partially recessive. Totally recessive alleles persist in low frequency for many generations, but result in relatively little impact on the population, depending on the number of mutated loci. We also applied population genetics concepts to assess the potential for heritable mutations induced by the Exxon Valdez oil spill in Prince William Sound, Alaska, to affect pink salmon populations. We stress that breeding units (e.g., streams with distinct spawning populations of salmon) must be considered individually to assess heritable genetic effects. For several streams impacted by the oil spill, there is inconsistency between observed egg mortality and that expected if lethal heritable mutations had been induced by exposure to crude oil. Observed mortality was either higher or lower than expected depending on the spawning population, year, and cohort considered. Any potential subtle effect of lethal mutations induced by the Exxon Valdez oil spill is overridden by natural environmental variation among spawning areas. We discuss the need to focus on population-level effects in toxicological assessments because fish and wildlife management focuses on populations, not individuals.

Mutagenicity oil-induced mutations toxicity pink salmon (Oncorhynchus gorbuscha) Exxon Valdez oil spill 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adkison, M.D. (1995) Population differentiation in Pacific salmon: local adaptation, genetic drift, or the environment? Can. J. of Fish. Aquatic Sci. 52, 2762–77.Google Scholar
  2. Allendorf, F.W. (1978) Protein polymorphism and the rate of loss of duplicate gene expression. Nature 272, 76–8.PubMedGoogle Scholar
  3. Allendorf, F.W. and Phelps, S.R. (1981) Use of allelic frequencies to describe population structure. Can. J. of Fish. Aquatic Sci. 38, 1507–14.Google Scholar
  4. Allendorf, F.W. and Thorgaard, G.H. (1984) Tetraploidy and the evolution of salmonid fishes. In Turner, B., ed. Evolutionary Genetics of Fishes, pp. 1–53. New York: Plenum.Google Scholar
  5. Ashby, J. (1982) Screening chemicals for mutagenicity: practices and pitfalls. In Heddle, J.A., ed. Mutagenicity: New Horizons in Genetic Toxicology, pp. 2–33. New York: Academic Press.Google Scholar
  6. Aspinwall, N. (1974) Genetic analysis of North American populations of pink salmon, Oncorhynchus gorbuscha, possible evidence for the neutral mutation B random drift hypothesis. Evolution 28, 295–305.Google Scholar
  7. Barnthouse, L.W. (1993) Population-level effects. In Suter, G.W., ed. Ecological Risk Assessment, Chapter 8. Chelsea, Michigan: Lewis Publishers.Google Scholar
  8. Bickham, J.W., Mazet, J.A., Blake, J., Smolen, M. J., Lou, Y. and Ballachey, B. E. (1998) Flow-cytometric determination of genotoxic effects of exposure to petroleum in mink and sea otters. Ecotoxicology 7, 191–9.Google Scholar
  9. Bickham, J.W. and Smolen, M.J. (1995) Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environmental Health Perspectives 102, Suppl. 12, 25–8.Google Scholar
  10. Blaylock, B.G. and Frank, M.L. (1980) Effects of chronic low-level irradiation on Gambusia affinis. In Egami, N., ed., Radiation Effects on Aquatic Organisms, pp. 81–90. Tokyo: Japan Sci. Soc. Press.Google Scholar
  11. Brannon, E.L., Moulton, L.L., Gilbertson, L.G., Maki, A.W. and Skalski, J.R. (1995) An assessment of oil spill effects on pink salmon populations following the Exxon Valdez oil spill. Part 1: Early life history. In Wells, P.G., Butler, J.N. and Hughes, J.S. eds. Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters, ASTM STP 1219, pp. 548–84. Philadelphia: American Society for Testing and Materials.Google Scholar
  12. Brannon, E.L. and Maki, A.W. (1996) The Exxon Valdez oil spill: Analysis of impacts on the Prince William Sound pink salmon. Reviews in Fisheries Science 4, 289–337.Google Scholar
  13. Brannon, E.L. (1998) The assessment of pink salmon incubation success in Prince William Sound following the Exxon Valdez oil spill. In Ryall, P.J. and Ryan, A.C. eds. In Proceedings of the 18th Northeast Pacific Pink and Chum Salmon Workshop, pp. 65–76. Canada Nanaimo, British Columbia: Dept. of Fisheries and Oceans.Google Scholar
  14. Brown E.D., Baker, T.T., Hose, J.E., Kocan, R.M., Marty, G.D., McGurk, M.D., Norcross, B.L. and Short, J. (1996) Injury to the early life history stages of Pacific herring in Prince William Sound after the Exxon Valdez oil spill. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 448–62. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  15. Bue, B.G., Sharr, S., Moffit, S.D. and Craig, A.K. (1996) Effects of the Exxon Valdez oil spill on pink salmon embryos and preemergent fry. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 619–27. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  16. Carls, M.G., Wertheimer, A.C., Short, J.W., Smolowitz, R.M. and Stegeman, J.J. (1996) Contamination of juvenile pink and chum salmon by hydrocarbons in Prince William Sound after the Exxon Valdez oil spill. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 593–618. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  17. Caro, T.M. and Laurenson, M.K. (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263, 485–6.PubMedGoogle Scholar
  18. Caughley, G. and Sinclair, A.R.E. (1994) Wildlife Ecology and Management. Oxford: Blackwell Scientific Publications.Google Scholar
  19. Clark, R.C., Jr. and Brown, D.W. (1977) Petroleum: properties and analyses in biotic and abiotic systems. In Mallins, D.C., ed. Effects of Petroleum on Arctic and Subarctic Marine Environments, pp. 1–89. New York: Academic Press.Google Scholar
  20. Clark, A.G., Feldman, M.W. and Christiansen, F.B. (1981) The estimation of epistasis in components of fitness in experimental populations of Drosophila melanogaster Part I: A two-stage maximum likelihood model. Heredity 46, 321–46.PubMedGoogle Scholar
  21. Collier, T.K., Krone, C.A., Krahn, M.M., Stein, J.E., Chan, S.L. and Varanaski, U. (1996) Petroleum exposure and associated biochemical effects in subtidal fish after the Exxon Valdez oil spill. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 671–83. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  22. Cronin, M.A. and Wilson, W.J. (1998) Crude oil and heritable mutations: An assessment of the Exxon Valdez oil spill impacts on pink salmon populations. In Ryall, P.J. and Ryan, A.C., eds. Proceedings of the 18th Northeast Pacific Pink and Chum Salmon Workshop, pp. 45–56. Nanaimo, British Columbia: Dept. of Fisheries and Oceans Canada.Google Scholar
  23. Custer, T. W., Bickham, J.W., Lyne, T.B., Lewis, T., Ruedas, L.A., Custer, C.M. and Melancon, M.J. (1994) Flow cytometry for monitoring contaminant exposure in black-crowned nightherons. Arch. Environ. Contam. Toxicol. 27, 176–9.PubMedGoogle Scholar
  24. Denissenko, M.F., Pao, A., Tang, M. and Pfeifer, G.P. (1996) Preferential formation of benzoapyrene adducts at lung cancer mutational hotspots in P53. Science 274, 430–2.PubMedGoogle Scholar
  25. Ellenton, J.A. and Hallett, D.J. (1981) Mutagenic and chemical analysis of aliphatic and aromatic fractions of Prudhoe Bay crude oil and fuel oil no. 2. Journal of Toxicology & Environmental Health 8, 959–72.Google Scholar
  26. Endler, J.A. (1986) Natural Selection in the Wild. Princeton, New Jersey: Princeton University Press.Google Scholar
  27. Falconer, D.S. (1989) Introduction to Quantitative Genetics. 3rd Ed. New York: John Wiley & Sons, Inc.Google Scholar
  28. Fritz, A., Rozowski, M., Walker, C. and Westerfield, M. (1996) Identification of selected gamma-ray induced deficiencies in zebrafish using multiplex polymerase chain reaction. Genetics 144, 1735–45.PubMedGoogle Scholar
  29. Geiger, H.J., Bue, B.G., Sharr, S., Wertheimer, A.C. and Willette, T.M. (1996) A life history approach to estimating damage to Prince William Sound pink salmon caused by the Exxon Valdez oil spill. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 487–98. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  30. Gharrett, A.J., Smoot, C. and McGregor, A.J. (1988) Genetic relationships of even-year Northwestern Alaskan pink salmon. Transactions of the American Fisheries Society 117, 536–45.Google Scholar
  31. Gilbert, F.F. and Dodds, D.G. (1992) The Philosophy and Practice of Wildlife Management. Malabar, Florida: Krieger Publishing Company.Google Scholar
  32. Guerin, M.R., Clark, B.R., Ho, C.-H., Epler, J.L. and Rao, T.K. (1978) Short-term bioassay of complex organic mixtures. Part 1. Chemistry. In Waters, M.D., Nesnow, S., Huisingh, J.L., Sandhu, S.S. and Claxton, L., eds. Application of Short-term Bioassays in the Fractionation and Analysis of Complex Environmental Mixtures, pp. 247–68. New York: Plenum.Google Scholar
  33. Guerin, M.R., Ho, C.-H, Rao, T.K., Clark, B.R. and Epler, J.L. (1980) Polycyclic aromatic primary amines as determinant chemical mutagens in petroleum substitutes. Environmental Research 23, 42–53.PubMedGoogle Scholar
  34. Guerin, M.R., Rubin, I.B., Rao, T.K., Clark, B.R. and Epler, J.L. (1981) Distribution of mutagenic activity in petroleum and petroleum substitutes. Fuel 60, 282.Google Scholar
  35. Harris, C.C. (1993) p53: At the crossroads of molecular carcinogenesis and risk assessment. Science 262, 1980–1.Google Scholar
  36. Hartl, D.L. and Clark, A.G. (1989) Principles of Population Genetics. Sunderland, Massachusetts: Sinauer Associates, Inc.Google Scholar
  37. Hemsworth, B.N. and Wardhaugh, A.A. (1978) The induction of dominant lethal mutations in Tilapia mossambica by alkane sulphonic esters. Mutation Res. 58, 263–8.PubMedGoogle Scholar
  38. Hilborn, R. (1996) Detecting population impacts from oil spills: a comparison of methodologies. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 639–44. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  39. Holloway, M. (1996) Sounding out science. Scientific American, 106–12.Google Scholar
  40. Hom, T., Varanasi, U., Stein, J.E., Sloan, C.A., Tilbury, K.L. and Chan, S.L. (1996) Assessment of the exposure of subsistence fish to aromatic compounds after the Exxon Valdez oil spill. In Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. Proceedings of the Exxon Valdez Oil Spill Symposium, pp. 856–66. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  41. Hose, J.E., McGurk, M.D., Marty, G.D., Hinton, D.E., Brown, E.D. and Baker, T.T. (1996) Sublethal effects of the Exxon Valdez oil spill on herring embryos and larvae: morphological, cytogenetic, and histopathological assessments, 1989–1991. Can. J. Fish. and Aquatic Sci. 53, 2355–2365.Google Scholar
  42. Kligerman, A.D. (1982) Fishes as biological detectors of the effects of genotoxic agents. In J.A. Heddle, ed. Mutagenicity: New Horizons in Genetic Toxicology, pp. 435–57, New York: Academic Press.Google Scholar
  43. Lamb, T., Bickham, J.W., Gibbons, J.W., Smolen, M.J. and McDowell, S. (1991) Genetic damage in a population of slider turtles (Trachemyus scripta) inhabiting a radioactive reservoir. Arch. Environ. Contam. Toxicol. 20, 138–42.PubMedGoogle Scholar
  44. Lande, R. (1988) Genetics and demography in biological conservation. Science 241, 1455–60.PubMedGoogle Scholar
  45. Lockard, J.M., Prater, J.W., Viau, C.J., Enoch, H.G. and Sabharwal, P.S. (1982) Comparative study of the genotoxic properties of eastern and western U.S. shale oils, crude petroleum, and coalderived oil. Mutation Research 102, 221–35.PubMedGoogle Scholar
  46. Loughlin, T.R. ed. (1994) Marine Mammals and the Exxon Valdez. New York: Academic Press.Google Scholar
  47. MacLean, J.A. and Evans, D.O. (1981) The Stock concept, discreteness of fish stocks, and fisheries management. Can. J. Fish. Aquatic Sci. 38, 1889–98.Google Scholar
  48. Maki, A.W. and Parker, K.R. (1996) An analysis of post-spill spawning by pink salmon in selected Prince William Sound streams through 1994. In Fuss, H. and Graves, G. eds. Proceedings of the 17th Northeast Pacific Pink and Chum Salmon Workshop, pp. 156–63. Olympia Washington: Northwest Indian Fisheries Commission and Washington Department of Fish and Wildlife.Google Scholar
  49. Maki, A.W., Brannon, E.J., Gilbertson, L.G., Moulton, L.L. and Skalski, J.R. (1995) An assessment of oil spill effects on pink salmon populations following the Exxon Valdez Oil Spill. Part 2: Adults and escapement. In Wells, P.G., Butler, J.N. and Hughes, J.S. eds. Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters, ASTM STP 1219, pp. 585–625. Philadelphia: American Society for Testing and Materials.Google Scholar
  50. Malkin, D. (1994) Germline p53 mutations and heritable cancer. In Campbell, A., Anderson, W. and Jones, E.W., eds. Annual Review of Genetics, pp. 443–65.Google Scholar
  51. McBee, K. and Bickham, J.W. (1988) Petrochemical-related DNA damage in wild rodents detected by flow cytometry. Bulletin of Environmental Contamination and Toxicology 40, 343–9.PubMedGoogle Scholar
  52. Medica, P.A., Turner, F.B. and Smith, D.D. (1973) Effects of radiation on a fenced population of horned lizards (Phrynosoma platyrhinos) in southern Nevada. Journal of Herpetology 7, 79–85.Google Scholar
  53. Miller, G.D., Seeb, J.E. and Bue, B.G. (1994) Saltwater exposure at fertilization induces ploidy alterations, including mosaicism, in salmonids. Can. J. Fish. Aquatic Sci. 51, 42–9.Google Scholar
  54. Moulton, L.L. (1998) Pink Salmon escapement trends in selected Prince William Sound streams through 1996. In Ryall, P.J. and Ryan, A.C., eds. Proceedings of the 18th Northeast Pacific Pink and Chum Salmon Workshop, pp. 57–64. Nanaimo, British Columbia: Dept. of Fisheries and Oceans Canada.Google Scholar
  55. Neel, J.V., Satoh, C., Goriki, K., Fujita, M., Takahashi, N., Asakawa, J. and Hazama, R. (1986) The rate with which spontaneous mutation alters the electrophoretic mobility of polypeptides. Genetics 83, 389–93.Google Scholar
  56. Neel, J.V., Satoh, C., Goriki, K., Asakawa, J., Fujita, M., Takahashi, N., Kageoka, T. and Hazama, R. (1988) Search for mutations altering protein charge and/or function in children of atomic bomb survivors: final report. Am. J. Hum. Genet. 42, 663–76.PubMedGoogle Scholar
  57. Overton, E.B., Sharp, W.D. and Roberts, P. (1994) Toxicity of petroleum. In Cockerham, L.G. and Shane, B.S., eds. Basic Environmental Toxicology, pp. 133–56. Boca Raton: CRC Press.Google Scholar
  58. Paine, R.T., Ruesink, J.L., Sun, Ad., Soulanille, E.L., Wonham, M.J., Harley, C.D.G., Brumbaugh, D.R. and Secord, D.L. (1996) Trouble on oiled waters: lessons from the Exxon Valdez oil spill. Annu. Rev. Ecol. Syst. 27, 197–235.Google Scholar
  59. Pelroy, R.A., Sklarew, D.S. and Downey, S.P. (1981) Comparison of mutagenicity of fossil fuels. Mutation Research 90, 233–45.PubMedGoogle Scholar
  60. Rice, S.D., Spies, R.B., Wolfe, D.A. and Wright, B.A., eds. (1996) Proceedings on the Exxon Valdez Oil Spill Symposium. Bethesda: American Fisheries Society Symposium 18.Google Scholar
  61. Seeb, J. E., Habicht, C., Greene, B., Kretschmer, E., Olsen, J.B. and Evans, D. (1996) Laboratory examination of oil-related embryo mortalities that persist in pink salmon populations in Prince William Sound. Exxon Valdez Oil Spill Restoration Project Annual Report (Restoration Project 95191A-2). Anchorage, AK: Alaska Department of Fish and Game.Google Scholar
  62. Sharr, S., Bue, B.G., Moffitt, S.D., Craig, A.K. and Evans, D.G. (1994a) Injury to salmon eggs and preemergent fry in Prince William Sound. Exxon Valdez Oil Spill State/Federal Natural Resource Damage Assessment Final Report (Fish/Shellfish Study Number 2), Alaska Department of Fish and Game.Google Scholar
  63. Sharr, S., Seeb, J.E., Bue, B.G., Craig, A.K. and Miller, G.D. (1994b) Injury to salmon eggs and preemergent fry in Prince William Sound, Exxon Valdez Oil Spill State/Federal Natural Resource Damage Assessment Final Report (Restoration Study 60C), Alaska Department of Fish and Game.Google Scholar
  64. Sharr, S., Seeb, J.E., Bue, B.G., Craig, A. and Miller, G.D. (1994c) Injury to salmon eggs and preemergent fry in Prince William Sound, Exxon Valdez Oil Spill State/Federal Natural Resource Damage Assessment Final Report (Restoration Project 93003). Cordova, AK: Alaska Department of Fish and Game.Google Scholar
  65. Sheppard, E.P., Wells, R.A. and Georghiou, P.E. (1983) The mutagenicity of a Prudhoe Bay crude oil and its residues from an experimental in situ burn. Environmental Research 30, 427–41.PubMedGoogle Scholar
  66. Simmons, M.J. and Crow, J.F. (1977) Mutations affecting fitness in Drosophila populations. Annu. Rev. Genetics 11, 49–78.Google Scholar
  67. Sommer, S.S. (1995) Recent human germ-line mutation: inferences from patients with hemophilia B. TIG 11, 141–7.PubMedGoogle Scholar
  68. Wallace, B. (1963) The elimination of an autosomal lethal from an experimental population of Drosophila melanogaster. American Naturalist 97, 65–6.Google Scholar
  69. Waples, R.S. and Teel, D.J. (1990) Conservation genetics of Pacific salmon. I: Temporal changes in allele frequency. Conservation Biology 4, 144–56.Google Scholar
  70. Wells, P.G., Butler, J.N. and Hughes, J.S., eds. (1995) Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters. ASTM STP 1219. Philadelphia: American Society for Testing and Materials.Google Scholar
  71. Wiens, J.A. (1996) Oil, seabirds, and science: The effects of the Exxon Valdez oil spill. BioScience 46, 587–97.Google Scholar
  72. Wirgin, I.I. and Garte, S.J. (1994) Assessment of environmental degradation by molecular analysis of a sentinel species: Atlantic tomcod. In S.J. Garte, ed. Molecular Environmental Biology, pp. 117–32, Florida: CRC Press, Inc.Google Scholar
  73. Wyrobek, A.J. (1982) Sperm assays as indicators of chemically induced germ-cell damage in man. In J.A. Heddle, ed. Mutagenicity: New Horizons in Genetic Toxicology, pp. 337–50, New York: Academic Press.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Matthew A. Cronin
    • 1
  • John W. Bickham
    • 2
    • 3
  1. 1.LGL Alaska Research Associates, Inc.AnchorageUSA
  2. 2.Department of Wildlife and Fisheries SciencesTexas A & M University, College StationUSA
  3. 3.LGL Ecological Genetics, Inc.BryanUSA

Personalised recommendations